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Weight loss and body composition changes following three sequential cycles of ketogenic enteral nutrition
Gianfranco Cappello, Antonella Franceschelli, Annalisa Cappello, and Paolo De Luca
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Abstract
Background:
Materials and Methods:
Results:
Conclusion:
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INTRODUCTION
Obesity is a public health problem with worldwide effects. The presence
of obesity is associated with increased risk of death, especially from
cardiovascular causes and cancer.[1] Body mass index (BMI; weight in
kg/height in m2) is a strong predictor of obesity-associated mortality. Life
expectancy in obese patients is reduced such that patients with a BMI of
30-35 kg/m2 have a median survival reduced by 2-4 years; those with a
BMI of 40-45 kg/m2 have a median survival reduced by 8-10 years.[2]
Obesity is also associated with chronic illnesses, including diabetes,
hypertension, osteoarthritis, gallstones, gout to name a few,[3] as well as
reduced quality of life.[4] Adult obesity and overweight are responsible
for up to 6% of health care expenditures and 10-13% of deaths in the
European Region; in addition, they impose indirect costs (due to the loss
of lives, productivity and related income) that are at least two times
higher.[5]
In several randomized controlled trials, a low-carbohydrate, ketogenic
diet (LCKD) has resulted in significant weight loss over a 6- to 12-month
period.[6,7,8] Moreover, recent studies suggest that an LCKD results in
less hunger,[9,10,11] seems to be safe even in the long term[12,13] and
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preserves lean mass even during hypo energetic conditions of weight
loss,[14,15] although there is still not enough evidence for a full
consensus on the use of this kind of diet.[16]
The aim of this study was to evaluate retrospectively body composition
changes and the efficacy and safety of an LCKD supplied via nasogastric
tube, called ketogenic enteral nutrition (KEN). KEN is a short-term
treatment for obesity developed in our Department of Surgery Paride
Stefanini of the University La Sapienza in Rome. The KEN diet is a
modified LCKD similar to the protein sparing modified fast (PSMF). In
essence, the PSMF diet is a low-calorie diet that is high in protein (1.2 g
of protein per kg of ideal body weight) in the form of lean meat, fish, or
fowl,[17] i.e., foods that are naturally rich in high quality proteins but
low in fats and very low in carbohydrates. Like the PSMF diet, the KEN
diet can be performed at home and both diets promote moderate ketosis
in all patients. However, the KEN diet differs from the PSMF diet in
several key points;[17]
Protein intake is supplemented continuously both day and night via
infusion through a small nasogastric tube. This ensures a steady
protein intake at all times, avoids the unpleasant taste of less-
palatable proteins and allows a more effective control of protein
intake.
Daily protein intake is reduced to 50 g for women and 65 g for men
(an average of 0.86 g/kg of ideal body weight) considering that we
are using only high biological value protein. Furthermore, with a
slow-flow tube infusion (2.1-2.7 g of protein/h) we can suppose
100% intestinal absorption.
Carbohydrate intake is completely eliminated; during each
treatment cycle patients are permitted to drink only water or tea
without sugar.
Length of treatment is reduced to a 10-day cycle. Patients can
repeat multiple cycles after a rest period of at least 10 days.
The aim of this study was to evaluate the safety of KEN treatment,
patient compliance, and efficacy with regard to weight loss and body
composition changes after three subsequent 10-day cycles of KEN
treatment.
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Methods and procedures
The study was performed within the Clinical Nutrition Service of the
Department of Surgery Paride Stefanini at the University La Sapienza in
Rome and included obese and overweight patients who did not have
success with previous dietetic treatments for obesity.
Exclusion criteria included pregnancy or lactation, type 1 diabetes, renal
failure, hepatic failure, heart failure, history of cardiac arrhythmias
and/or long QT syndrome, eating disorders and/or severe psychiatric
disturbances, and age < 16 or > 75 years. The patients were self-referred
and each patient had to sign an informed consent release before the
beginning of the treatment. The procedures were in accordance with the
Helsinki Declaration of 1975 (as revised in 1983).
The cases analyzed for this study were selected from a very large
population of more than 19,000 patients who received KEN treatment
during a 5-year period (from 2006 to 2011). From this pool we selected
only patients who underwent the first KEN cycle and then came back for
2 more subsequent cycles with rest periods of 10-13 days between each
treatment.
The patients’ ages varied from 16 to 74 years (with a mean age of 44.2
years) [Table 1]. The male:female ratio was 2:5. The average weight at
the start of the treatment for all patients was 114.8 kg and was higher for
men than women (135.9 kg versus 106.5 kg, respectively). The mean
BMI was 41.2 kg/m2 (obesity class 3) and was also higher in the men
than in the women (43.8 kg versus 40.1 kg). The men had a very high
body cell mass (BCM) compared with the women (45.5 kg versus 29.4
kg), however, the average fat mass (FM) was nearly the same for men
and women (50.3 kg versus 49.3 kg).
Table 1
Baseline anthropometric profiles of the patients by gender. The results
are presented as mean (SD)
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Each patient had been received a medical visit before the beginning
treatment and during the treatment cycles that were domiciliary, a
medical doctor (MD) was available by telephone 24 h/day. At the
beginning of each cycle the patients received a 6-fr polyurethane tube
inserted through the nose. The tube was held in place on the patient's
cheek and ear by transparent tape.
The patients were given a short course to educate them about using the
infusion pump. The infusion rate was controlled by a small peristaltic
pump providing a daily dose of 50 g of protein for women and 65 g for
men (resulting in an average of 0.85 g/kg of ideal body weight in women
and 0.89 g/kg in men) and 13-17 mEq of potassium [Table 2]. In
addition, each patient received a supplement providing the RDA for all
vitamins and essential minerals except calcium and phosphorus. They
were also given a 50-g dose of Macrogol 4000 to be taken on the first,
fourth and seventh days of treatment in order to make up for the absence
of fibers in the protein solution.
Table 2
Composition of the KEN diet. The whey proteins and hydrolyzed
collagen in the solution are of bovine origin and potassium chloride was
used
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We decided to administer the feeding formula via a nasogastric tube for
two reasons, namely because the formula is not highly palatable and also
providing food continuously throughout the day helped reduce hunger.
The treatments were administered over 10 days for every patient as this
time period is free from the hazards associated with long-term liquid
protein diets.[18,19] During treatment cycles the patients were not
allowed to eat anything by mouth, and they were asked to drink only
water or other unsweetened beverages ad libitum.
Every day during the cycle the patients were asked to monitor their level
of Ketonuria by using the Ketur test. Patients affected by hypertension
were suggested to reduce or to stop their usual medication to avoid
symptomatic hypotension, to control daily their blood pressure and to
contact the MD in case of increa sed blood pressure. Even diabetic
patients were suggested to reduce or stop their usual medications to
avoid hypoglycemia. They were also asked to monitor glycemia 3 times
a day and to contact the MD in case of blood glucose > 160 mg%.
Patients affected by gout and/or hyperuricemia were supplied with daily
doses of allopurinol.
Measurements of body weight and bioimpedance (using a Handy 3000
DS Medica, single frequency, 50Khz) as well as clinical and laboratory
data were taken at the beginning and at the end of the KEN cycles. The
body composition was calculated by a computerized program which was
provided by the manufacturer, according to the three-compartment
model.[20]
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After each 10-day KEN treatment, patients returned to the unit for tube
removal, to report all treatment data (daily evaluation of hunger level,
body weight and ketonuria) and to undergo another body composition
evaluation. Between cycles, each patient was given a rest period during
which he/she would be advised to follow a low–carbohydrate, normal
caloric diet. After this 10-day rest period they returned for a new
assessment of body composition before beginning the next treatment
cycle.
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RESULTS
Ketonuria was observed in most patients by the second day of KEN
treatment and increased within 2-3 days to 100-120 mg%. Commonly the
Ketonuria was accompanied by moderate halitosis; however, this did not
prevent the patients from carrying out normal daily activities.
By the fifth day of treatment 24% of patients reported a strong sense of
asthenia, even if they had normal blood pressure levels. By the end of the
treatment, 12% of patients reported a mild sense of hunger.
Laboratory examinations revealed moderate hyper-cholesterolemia in
35% of the patients at baseline; the values did not change after KEN
therapy. Nearly one quarter (22%) of the patients were diabetic and
receiving treatment for their condition at the start of treatment. As
reported by other authors,[21] 92% of the diabetics in our study had to
suspend their medications during the treatments period because the lack
of carbohydrate in the nutritional solution was sufficient to lower their
glycemia on its own. Of these patients, who suspended anti-diabetic
therapy, 22% reported glucose values as low as 50-60 mg/dL, but no
cases of hypoglycemia were reported. Similarly, 80% of hypertensive
patients also suspended their medication because the KEN treatment had
a very powerful anti-hypotensive effect. Reduced hypertension during
and after PSMF has been reported by Dornfeld.[22]
After three 10-day KEN cycles, patients lost an average of 14.4 kg of
body weight [Figure 1], 3.5 kg of BCM, 10.6 kg of FM, and 2.6 kg of
TBW [Figure 2]. The weight loss was higher in male patients (18.1 kg in
males versus 12.9 kg in females) but female patients lost a higher
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percentage of FM (76% in females versus 62% in males). Fat mass
decreased not only during KEN cycles but also during the rest periods.
Figure 1
Weight change during 3 cycles of KEN (green) and 3 rest periods (red) of 10-13
days. Total weight loss is 14.4 kg, 12.5% of the initial body weight. Student's
paired t-test was used for the statistical analysis
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Figure 2
Body composition changes (in kg) after three cycles of KEN therapy and 10 days
of follow-up. The patients lost 3.5 ± 3.3 kg of BCM and 10.6 ± 3.7 kg of fat.
(KEN-Ketogenic Enteral Nutrition; TBW-Total body water; FM-Fat mass; BCM-
Body cell mass)
Treatment complications:
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All patients received the same amount of protein during the treatments:
50 g/d for women and 65 g/d for men, corresponding to an average of
1.67 ± 0.3 g of protein/kg of BCM/day. To compare the positive
predictive value of loss of fat mass and sparing of BCM, we split the
patients into two groups [Table 3]. One group consisting of 105 patients
who received less than 1.67 g protein/kg of BCM/day (group A,
receiving an average of 1.45 g protein/kg of BCM/day) and a second
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group of 83 patients who received more than 1.67 g protein/kg of
BCM/day (group B, receiving an average of 1.95 g protein/kg of
BCM/day). Table 3 shows the results from these two groups. Percent
weight loss was similar between the groups, but group B showed
significantly less reduction to BCM.
Table 3
Comparison between patients who were infused with 1.45 g of protein/kg
of BCM (Group a) and patients who were infused with 1.9 g of protein
(Group b)
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DISCUSSION
KEN is a well-tolerated treatment that produces significant, rapid weight
loss. This gives the patient a psychological boost because he/she sees
immediate results. Few patients were not able to tolerate the nasal tube
(0.03%) or had problems with the nutritional pump (4%). This is
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important because the nasal intubation and pump system are essential to
control the intake of proteins during both day and night to avoid the
catabolism of lean mass during the treatment period.
After three 10-day KEN cycles, patients lost an average of 12.5% of their
initial body weight. Judging from the changes in body composition, loss
of FM accounted for 73.9% of the weight loss while BCM loss
accounted for 24.1%. Interestingly, while the loss of BCM is only during
KEN cycles, the loss of fat continues after the end of KEN therapy. It is
unclear why FM continued to decline despite overall body weight
increased during the normal caloric feeding period of the 10-day follow-
up. One possible explanation for the effect on FM may be that to assess
accurately water content after the rapid weight loss we should wait a few
days for the stabilization of body compartments. We know that
bioimpedance does not measure fat directly; rather, it measures BCM
and extracellular water and by subtracting these two values from total
body weight the remainder is assumed to be FM. Because of this
assumption, any underestimation of body water will be reported as an
increase of FM, and the actual reduction of fat will not be accounted for
at that time. After the stabilization of water compartments an apparent
additional loss of fat will be registered. This mechanism may justify the
reported data and account for bioimpedance inaccuracies in patients
rapidly gaining or losing FM.
The significant difference in BCM loss in the patients given 1.45 g of
protein/kg of BCM compared with those given 1.95 g of protein indicates
optimal results can be obtained by infusing each patient with the higher
amount of protein proportional to initial BCM.
If we compare the results of this study with other PSMF studies we find
that weight loss after 17 weeks of PSMF reported by Palgi[23] was 21 kg
versus 14.4 kg in 3 weeks of the present study. Van Gaal[24] results are
closer to our results: 15 patients with 6 weeks of PSMF with a
lactalbumin derived containing 60 g/day protein lost 14.4 kg.
Wadden[25] patients lost around 8 kg in 4 weeks either using a lean
meat, fish, and fowl 450 kcal diet or an isocaloric protein-formula-liquid
diet. All these authors do not report of any significant clinical
complications. Wadden found that a liquid formula diet given by mouth
was less tolerated than a food diet. Comparing these PSMF studies with
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our results we find out that our patients lost more weight in less time and
probably this is due to the fact that using a 24 h infusion we could reduce
protein intake always sparing BCM mass. This is the main rationale
behind the tube infusion.
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CONCLUSION
This study demonstrates that KEN therapy administered over 10-day
cycles can induce rapid weight loss; in this sample of 188 obese patients
we obtained a 12.5% total weight loss, 73.9% of which was FM.
Comparing with other PSMF studies weight loss is increased. KEN
therapy can also be used to treat diabetic and/or hypertensive patients,
but their therapies have to be reformulated during the treatment period.
The nasal tube is well-tolerated and complications during the nasal
insertion and treatment are very low and generally tolerable.
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Footnotes Source of Support: Nil
Conflict of Interest: None declared.
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